1

Food Bioprocess Technol (2010) 3:2435

DOI 10.1007/s11947-009-0189-8

REVIEW PAPER

Emerging Bacterial Pathogens in Meat and Poultry:

An Overview
Montserrat Mor-Mur & Josep Yuste

Received: 12 September 2008 / Accepted: 22 January 2009 / Published online: 13 February 2009
# Springer Science + Business Media, LLC 2009

Abstract Many foodborne diseases are associated with

consumption of meat and poultry. Some pathogens were
not previously known (new pathogens), others have newly
arisen as foodborne (emerging pathogens), and others have
become more potent or associated with other products
(evolving pathogens). Many of these pathogens may cause
severe illness, besides gastroenteritis. Campylobacter jejuni
is a leading cause of food-associated bacterial illness;
Campylobacter jejuni O:19 and other serotypes are common etiological agents of GuillainBarr syndrome, a
neuropathy due to autoimmune response. Salmonella
Typhimurium DT104 and other serotypes have been found
to be multi-drug resistant; salmonellosis may lead to
chronic reactive arthritis. Many outbreaks of enterohemorrhagic Escherichia coli have been associated with consumption of undercooked contaminated ground beef;
complication may occur (e.g., hemolytic uremic syndrome
and thrombotic thrombocytopenic purpura). Listeria monocytogenes is ubiquitous; listeriosis is of major public health
concern because of the severity and non-enteric nature of
the disease (meningitis or meningoencephalitis, septicemia,
and abortion) and its ability to multiply at refrigeration
temperature. Arcobacter butzleri is a potential foodborne
pathogen, and has been isolated from raw poultry, meat,
and meat products; but its role in causing human illness is
not fully understood. Mycobacterium avium subsp. paratuberculosis can be transmitted by ingestion of raw and
processed meats; the organism may contribute to Crohns
M. Mor-Mur (*) : J.
Yuste
CER Planta de Tecnologia dels Aliments (XaRTA, XIT),
Departament de Cincia Animal i dels Aliments,
Facultat de Veterinria, Universitat Autnoma de
Barcelona,
08193 Bellaterra,
Barcelona, Spain
e-mail: montserrat.mor-mur@uab.es

disease, a chronic intestinal enteritis. Beef, pork, lamb, and/

or poultry have been reported as sources of infection for the
abovementioned organisms but have not been generally
associated with disease outbreaks of some of the pathogens.
Keywords New, emerging and evolving foodborne
pathogens . Pathogenic bacteria . Meat . Poultry .
Food safety . Food policy

Introduction
The term emerging pathogens means that the present
strains are adapting for survival to stresses in new environments. But three different concepts should be considered:
new, evolving, and emerging pathogens. New foodborne
pathogens are those that were not previously described and
are serious hazards for public health and important causal
agents of outbreaks. Evolving foodborne pathogens are
those that become more potent (e.g., microorganisms whose
involvement in foodborne outbreaks was erroneously
thought to decrease, however, which are still implicated in
a considerable number of outbreaks) or become associated
with other products, and also those that have caused
diseases which have been erroneously attributed to other
foodborne pathogens for many years (e.g., microorganisms
that were already known but not recognized as causes of
human illnesses, that is, organisms whose pathogenicities
were unknown or neglected until now). Emerging foodborne pathogens are those that have newly arisen, that is,
they have been recognized pathogens for many years and
now have been associated with foodborne transmission
(Meng and Doyle 1998; Sofos 2008).
The most prevalent and serious emerging pathogens of
meat, poultry, and derived products are Campylobacter

jejuni, Salmonella Typhimurium DT104, Escherichia coli

O157:H7 and other enterohemorrhagic E. coli (EHEC),
Listeria monocytogenes, Arcobacter butzleri, Mycobacterium avium subsp. paratuberculosis, Aeromonas hydrophila,

Table 1 Programs for integration and improvement of epidemiological monitoring

Program

Website

and prions.
A public health concern associated with pathogenic
bacteria is the increased incidence of strains that are
resistant to antimicrobial agents. Those resistant microorganisms can be disseminated via animal feces to other
animals. Antibiotic resistance can be conferred by
mutational alteration or modification of target molecules, repression of uptake systems, activation of efflux
pumps, and inactivation of the antibiotic. Resistance to
antimicrobials is connected with genetic mechanisms.
Genes coding for bacterial resistance to one or several
antibiotics are often located in transposons or plasmids.
The use of a single antibiotic can select resistance to
that antibiotic and to other antibiotics, whose genes

UE Basic
Surveillance
Network (BSN)
Unexplained
Death and Critical
Illnesses Project
a
(UNEX)
WHO Global
Salm-Surv (GSS)
CDCs Emerging
Infections Program
Foodborne Diseases
Active Surveillance
Network (FoodNet)

https://www2.smittskyddsinstitutet.se/BSN/
main.jsp

reside in the same transposon or plasmid. The widespread use of antimicrobials in human and veterinary
medicine promotes the development of resistant strains
that can infect humans via the food chain. Therefore,
prudent use of antimicrobials may prolong the availability of effective drugs (Usera et al. 2002; Andersson
2003).
Developed countries have used for a long time
systems of surveillance of food safety problems.
However, many outbreaks of food poisoning are never
recognized because known pathogens are not accurately
diagnosed or reported, and other causative foodborne
agents are unknown and therefore unreported. This
causes underestimation of foodborne disease incidences.
Furthermore, industries check their products but usually
do not report positive findings (Todd 2003). Most
foodborne disease outbreaks and deaths with an undetermined cause are likely caused by known pathogens that
are not detected, particularly viruses, often members of the
Norovirus genus (Frenzen 2004). This situation can be
corrected through initiation of new and improvement of
existing epidemiological monitoring programs. Table 1
shows some interesting programs for integration and
improvement of epidemiological monitoring. There is a
need to institute and maintain effective surveillance and
control programs, including reliable and sufficiently
discriminative methods with rapid turn-around times, for
providing epidemiological information on foodborne
illness outbreaks and so reducing the prevalence of
pathogens. This requires a collective effort by public
health authorities. Furthermore, as most foodborne diseases
are due to mishandling of foods in ways we know we
should avoid (e. g., improper cooling, inadequate
heating/reheating, and poor personal hygiene), education of
food handlers and consumers about the importance of food
hygiene may improve safety and

so prevent many illnesses (Leon-Velarde et al. 2004; Yan et

al.
2005; Sofos 2008).
In some cases where a policy has been based on minimal
information about a food pathogen, with a more complete
understanding about that pathogen, the policy should be reevaluated and amended. Furthermore, regulations have to
be reviewed periodically considering, among others, progress in emerging pathogenic microorganisms in foodstuffs
and information from risk assessments (EC 2005).
Reliable tests for detection of pathogens may be
compromised by inappropriate specimen collection or
preparation procedures, or by antimicrobial therapy before
stool collection (Frenzen 2004). Likewise, recovery and
isolation methods may underestimate counts of pathogens,
because certain microorganisms resist cultivation on some
artificial media. Frequently, it is usual that a microorganism
is not initially recognized as a pathogen or a disease is not
connected with consumption of a contaminated food
because we do not know how to detect, isolate, and
characterize the organism. Problems with detection,
isolation, and character- ization are probably due to the
food structure and the culture media used. Molecular (i.e.,
PCR-based) diagnostic methods allow a better
differentiation among species, serotypes, or strains. Such
techniques are rapid, sensitive, and specific, which makes
them very useful tools to improve the diagnosis and to
understand the mechanisms implicated in pathogenic- ity,
resistance, and survival of the new strains described, and so
to know how to prevent or inactivate them. Among other
identification methods, immunological techniques and
anti- microbial resistance profiles have to be considered
(Leon- Velarde et al. 2004).
This work is an overview on the most important
emerging bacterial pathogens (that is, new, emerging, and
evolving pathogens) in meat, poultry, and derived
products.

http://www.cdc.gov/ncidod/dbmd/diseaseinfo/
unexplaineddeaths_t.htm
http://www.who.int/salmsurv/en
http://www.cdc.gov/foodnet

Hajjeh et al. (2002)

26
Food Bioprocess Technol (2010) 3:2435
Pathogenic Bacteria in Meat and Poultry
Many foodborne diseases are associated with consumption
of meat and poultry. Most of the chicken carcasses
currently on sale are contaminated with one pathogen or
another. The pathogens of greatest concern in fresh and
frozen meat and meat products are Salmonella spp.,
Escherichia coli O157:H7 and other enterohemorrhagic E.
coli (EHEC), L. monocytogenes, Staphylococcus aureus,
and the potential for Clostridium botulinum in cured hams
and sausages (Table 2). A substantial proportion of all
emerging infections is associated with farm animals and
meat. The most frequent outbreaks associated with consumption of contaminated poultry are caused by
Salmonella spp., S. aureus, and occasionally by Bacillus
cereus and psychrotrophic pathogens such as A.
hydrophila, L. mono- cytogenes, and Yersinia
enterocolitica (Table 2). Most of these pathogens cause
gastroenteritis. Campylobacter spp. are also a major cause
of bacterial enteritis, but they are not usually connected
with outbreaks due to erroneous diagno- sis or the
difficulties for detection and isolation of the pathogen
(Satin 2002; Ellerbroek 2004). Table 3 compiles a brief
description and some reported sources of infection by
emerging bacteria in meat and poultry. To supplement the
information gathered in that table, a model showing
potential risk of infections in the food chain and meat
safety is given in Fig. 1. This model could be useful for
farmers, producers, and consumers in understanding their
roles in preventing or reducing contamination of meat,
poultry, and derived products.
Fatal outbreaks of foodborne disease caused by E. coli
O157:H7 and L. monocytogenes have increased consumer
awareness and aroused interest by public health authorities
Table 2 Traditional versus emerging bacterial pathogens in meat
and poultry
Traditional pathogens

Emerging pathogens

Campylobacter spp.
Salmonella spp.
Escherichia coli
Yersinia enterocolitica
Staphylococcus aureus

Campylobacter jejuni (O:19, O:4,

O:1), Campylobacter lanienae
Salmonella Typhimurium (DT104,
DTU302), S. Enteritidis (PT4,
PT8, PT13, PT14b)
Enterohemorrhagic Escherichia
coli (EHEC)
Listeria
monocytogenes
Arcobacter butzleri
Mycobacterium avium
subsp. paratuberculosis
Aeromonas hydrophila
Enterobacter sakazakii
Helicobacter pylori,
Helicobacter pullorum

Clostridium perfringens
Clostridium botulinum
Bacillus cereus

Food Bioprocess Technol (2010) 3:2435

26

and the industry in improving sanitary conditions and

controlling pathogens in meat and poultry production and
processing. Strict farming, manufacturing, and hygienic
practices, consistent with an effective HACCP system, are
the basis for controlling pathogen contamination. Measures
concerning the production of microbiologically safe meat,
poultry, and derived products are divided into those guided
by the rigid legislative approach and those that follow a
more scientific approach based on risk analysis. Management of meat safety risks involves all sectors: from the
producer through the processor, distributor, packer, retailer,
food service worker, and consumer (Samelis et al. 2001;
Snijders and Collins 2004; Sofos 2008).
There is a relationship between the occurrence of E.
coli O157:H7 or Salmonella spp. or both in cattle feces
and the occurrence of these pathogens on derived
carcasses (McEvoy et al. 2004). Pathogens present in
feces are frequently transferred to the hide, which is a
major source of carcass contamination during dressing.
That transfer can be through cross-contamination during
transport and lairage. Bovine buccal cavity is also a source
for E. coli O157:H7 (Keen and Elder 2002). Thus, the
pathogen may be present at the beginning of the slaughter
process, and persist on meat cuts during fabrication. The
use of antimicrobial interventions (e.g., steam vacuuming
and chemical rinsing) are currently not encouraged in EU
abattoirs because they could be used to mask unacceptable
hygiene practice during slaughter operations (McEvoy et
al. 2004). European Food Safety Authority (EFSA)
Scientific Panels on Biological Hazards and on Food
Additives, Flavourings, Processing Aids and Materials in
Contact with Food evaluated and gave their opinions about
the
safety and
efficacy of
some antimicrobial
substances applied on poultry carcasses. The treatments
were found not to have toxicological risks to public
health. The panel on Biological hazards stated that
reduction of carcass surface spoilage microbiota could
favor the growth of Listeria spp. (EFSA 2005a, b).
Aerosols produced during dehiding, evisceration, and
carcass splitting are important sources of contamination.
Air circulated from heavily contaminated refrigeration coils
in meat and poultry processing plants is also a major
source. Absolute temperatures applied to carcasses and
rates at which they are achieved probably have important
effects on pathogen survival during chilling: heavier
carcasses contain more heat and cool more slowly than
smaller carcasses; in addition, carcasses with a thick fat
cover also cool more slowly (McEvoy et al. 2004).
A number of thermal and non-thermal (at sublethal
temperatures) procedures can be applied, alone or in
combination, for pathogen inactivation in meat, poultry,
and derived products (Table 4). For heat treatment, values
proposed are 62.8 C internal temperature for destruction of

Table 3 Description and sources of infection by the main emerging bacteria in meat and poultry
Emerging bacteria
Symptoms or diseases or both other than Reported sources of infection
usual enteric ones
Campylobacter jejuni (O:19, O:4, O:1), other Reactive arthritis, pancreatitis, meningitis,
Campylobacter spp.a
endocarditis, GuillainBarr and Miller
Fisher syndromes
Salmonella Typhimurium (DT104,
Chronic reactive arthritis
DTU302), Salmonella Enteritidis (PT4,
PT8, PT13, PT14b)b
Enterohemorrhagic Escherichia coli (E. coli Hemorrhagic colitis, hemolytic uremic
O157:H7, other serotypes of Shiga toxin- syndrome, thrombotic thrombocytopenic
c
purpura
producing E. coli)
Listeria monocytogenesd
Meningitis or meningoencephalitis,
septicemia, abortion
Arcobacter butzleri, other Arcobacter spp.
Mycobacterium avium subsp.
f
paratuberculosis
Aeromonas hydrophila, Aeromonas spp.g

Enterobacter sakazakiih
Helicobacter pylori, Helicobacter pullorumi

Raw and undercooked poultry and poultry products,

meat products
Poultry, eggs, roast beef, ham, pork sausage, salami
Undercooked ground beef, turkey roll, salami, roast
beef, venison jerky

Septicemia, bacteremia

Raw meats and meat products (salami), ready-to-eat

pork products, unreheated frankfurters, undercooked
chicken, organ meat
Raw poultry, pork and beef, meat products

Crohns disease

Raw and processed meats

Peritonitis, endocarditis, pneumonia,

conjunctivitis, urinary tract infections

Minced beef, pork, and chicken, smoked sausage,

liver pt, boiled ham
Minced beef, cured meats, sausage meat

Neonatal meningitis, bacteremia,

necrotizing enterocolitis, appendicitis,
conjunctivitis
Gastric ulcer and cancer, liver disease

Not reported

Altekruse et al. (1997), Chan et al. (2001), Gilbert and Slavik (2004), Inglis et al. (2004), Yan et al. (2005), Godschalk et al. (2006)

Meng and Doyle (1998), Tollefson et al. (1998), Echeita et al. (1999), Carlson (2004), Guerin et al. (2006), DAoust and Maurer (2007)

Meng and Doyle (1998), Juneja and Marmer (1999), Acheson (2003), Meng et al. (2007)

Hutchins (1996), Meng and Doyle (1998), Flodrops et al. (2005), Swaminathan et al. (2007)

Wesley (1997), Meng and Doyle (1998), Rivas et al. (2004), Lehner et al. (2005)

Hermon-Taylor (2001), Naser et al. (2004)

Galindo and Chopra (2007)

Iversen and Forsythe (2003), Gurtler et al. (2005)

Wesley (1997), Ceelen et al. (2006)

enteric pathogens such as Salmonella spp. and pathogenic

E. coli in roast beef (Van Schothorst 1998). Air chilling
leads to a slight microbial reduction at the surface, and is a
hygienic practice that avoids cross-contamination (Braun et
al. 2004). With ionizing radiation, the possibility of crosscontamination is greatly reduced. A 1.5-kGy treatment is
5
enough to give a 10 -fold E. coli O157:H7 reduction.
Ionizing radiation also markedly decreases the numbers of
Campylobacter spp., Salmonella spp. and other enterobacteria, and L. monocytogenes (Ross et al. 2003; Niemira
2008). The key motivation for beef ionizing radiation in the
USA was the presence of E. coli O157:H7 in ground beef.
Gamma irradiation combined with marination with natural
plant extract or with other chemical agents reduced the
radiation dose required for the complete inactivation of
Salmonella spp. and other pathogens in fresh meat and
poultry (Satin 2002; Ouattara et al. 2002). High pressure
processing makes it possible to pasteurize with no marked
changes in the nutrient content, odor, and taste. Further-

more, if pressurization is applied at mild or high temperature, the safety and shelf-life are enhanced (Cheftel and
Culioli 1997; Mor-Mur and Yuste 2003).
Active packaging can be used for meat and poultry
safety and preservation. Heat and gamma irradiation induce
cross-linking between protein molecules in the edible
coating film, and thus improve the properties of that film
by increasing its ability to retain the antimicrobial compound incorporated. The incorporation of ascorbic acid,
alone or in combination with cross-linked film coating,
considerably stabilized microbial growth in ground beef. A
cross-linked coating film formulated with plant essential
oils has been found to considerably decrease E. coli O157:
H7 counts. A negative aspect is that E. coli O157:H7 and
other bacteria seem to use certain edible coating films (e.g.,
milk protein-based film) as a substrate to sustain their
growth (Ouattara et al. 2002; Oussalah et al. 2004). Several
studies show the bacteristatic and bactericidal effects of
spices, condiments, and plant extracts. In particular, some

PRODUCTION AND PROCESSING

(INCLUDING SLAUGHTERING)

Implementation of HACCP and sanitary conditions

Safety of raw meat and poultry; undercooked ground
meat and poultry; fresh, minimally processed and readyto-eat meat and poultry products; unreheated frankfurters
Antimicrobial interventions (resistance to antimicrobials
by pathogenic microorganisms; and to low pH, heat, cold
temperature, dryness or low aw, and chemical additives)

FARM (ANIMAL PRODUCTION)

* Animal identification and

tracebility, and food product recalls
* Rapid and reliable pathogen
detection methodologies in laboratory

Animal health (zoonotic diseases),

welfare and human treatment
Antimicrobial interventions (increased
resistance of pathogens to antibiotics)
Food safety programs

DISTRIBUTION

Food handler training

Recontamination during slicing and packaging
Growth of organisms during storage
Consumer education

CONSUMER

Health problems
Improper preparation or consumption of
mishandled meat and poultry products
Increased virulence and/or resistance to
control and clinic treatment (human medicine)

Fig. 1 Model for meat and poultry safety

of these compounds (such as garlic, oregano, and cinnamon) have antibacterial activity against Salmonella Thypimurium, E. coli, and L. monocytogenes (Helander et al.
1998; Yuste and Fung 2002; Burt and Reinders 2003;
Table 4
inactivation

Treatments

for

bacterial

Physical treatments

Chemical treatments

Chilling
Freezing
Conventional heating
Microwave heating
Ohmic heating

Packaging:
Vacuum or modified atmosphere
(MAP), and/or
Active packaging (e.g., edible
coating films, containing ascorbic
acid, plant essential oils, and so on)

Ultrasound
Ultraviolet radiation
Ionizing radiation
High pressure processing
Pulsed electric fields
Oscillatory magnetic fields

(Spray) washing with water, steam,

or solutions (e.g., organic acids,
such as lactic acid, trisodium
phosphate)
Other agents in solution, such as
fatty acid esters, parahydroxybenzoic acid esters,
lysozyme, phenolic
compounds, isothiocyanates,
ascorbic acid
Nitrites
Sulfites
Spices, condiments, and plant
essential oils
Chitosan
Bacteriocins
Bacteriophages

Avila-Sosa et al. 2008). Spray washing with 10% of

trisodium phosphate results in considerable Salmonella
spp. and EHEC reductions. Washing with 2% of lactic acid
is also an effective treatment for surface decontamination
(Cutter and Rivera-Betancourt 2000). Enhanced survival
has been reported in meat plants at low temperatures, which
suggests a protective effect of the low storage temperature
on pathogenic bacteria (Samelis et al. 2001). Carcass
decontamination with water, steam, or chemical solutions
(e.g., organic acids) reduces surface contamination, but
pathogens surviving a particular stress (decontamination
treatments) may acquire cross-tolerance, proliferate, and
develop resistance and cross-protection to other stresses.
Persistent, stress-resistant pathogenic strains tend to develop and colonize abattoirs, and/or meat and poultry
processing and packaging plants, which increases food
safety risks (Samelis et al. 2001; McCann et al. 2006).

Campylobacter spp.
In contrast to the relatively low occurrence of outbreaks of
sidered
the leading cause
of sporadicspp.
bacterial
gastroentercampylobacteriosis,
Campylobacter
is currently
conitis, with C. jejuni being the most frequently implicated in
clinical diagnosis. In Canada and the UK, among many
other countries, the number of reported cases of campylobacteriosis exceeds the combined number of salmonellosis
and shigellosis cases. Between 1979 and 1987, C. jejuni
was implicated in 53 foodborne outbreaks in the USA,

affecting 1,547 individuals and resulting in two deaths.

Campylobacteriosis usually occur during the summer
months and involve diarrhea (sometimes bloody), fever,
and abdominal cramping as well as complications such as
reactive arthritis, pancreatitis, meningitis, endocarditis, and
GuillainBarr syndrome. The GuillainBarr syndrome is
a disorder of the peripheral nervous system, resulting in
acute flaccid paralysis, due to autoimmune response. It is
considered a sequela of C. jejuni-caused infections (Chan
et al. 2001; Gilbert and Slavik 2004; Yan et al. 2005; Ray
and Bhunia 2008). Campylobacter jejuni O:19 and other
serotypes (O:4, O:1) are some of the most common
etiological agents of GuillainBarr syndrome and its
variant Miller Fisher syndrome. The infective dose of C.
jejuni is quite low: less than 100 organisms can cause
disease (Meng and Doyle 1998; Acheson 2003; Godschalk
et al. 2006).
Raw and undercooked poultry are the primary sources
of a Campylobacter infection. A considerable portion of
broilers (88%) and poultry at retail (98%) has been found
contaminated with the pathogen. Epidemiologic studies
show that ca. 50% of sporadic cases of campylobacteriosis
are associated with handling or eating poultry. Meat
products can also contribute to illness (Meng and Doyle
1998; Chan et al. 2001; Inglis et al. 2004). Mead (2004)
reported that a decline in reported cases was associated
with new control measures in industries in the USA.
Campylobacter jejuni is carried in poultry intestinal
contents in high numbers, with infected chickens showing
few or no clinical signs of illness. This, compounded by a
prolonged period of shedding (ca.
43 days), results in fecal contamination of chicken
carcasses in processing plants and increases the risk of
transmission (Sahin et al. 2001; Inglis et al. 2004). Most
infections are associated with improper preparation or
consumption of mishandled poultry products (Altekruse et
al. 1997).
Campylobacter spp. are obligate microaerophiles and
most of them grow optimally at 42 C. Because of
difficulties in culturing the organism, in the past, Campylobacter outbreaks were reported as caused by unknown
agents or erroneously by other organisms, especially
Salmonella spp. Campylobacter spp. do not survive well
in food, and are relatively fragile and readily killed by heat
treatments (Meng and Doyle 1998). Campylobacter jejuni
has the ability to survive refrigeration and freezing, which
is of obvious relevance to food safety and public health.
Similar to other microorganisms, C. jejuni isolates can
produce stress proteins, which enhance the ability of the
organism to survive in adverse environments. Therefore,
refrigeration and freezing may constitute a powerful
selection for cold tolerance in poultry-derived strains.
Isolates producing elevated levels of stress proteins probably survive poultry processing better (Chan et al. 2001;
Gilbert and Slavik 2004).

There is a need for strategies to control C. jejuni

infection in the poultry reservoir and consequently reduce
the risk of human campylobacteriosis. The possibility of
animal vaccination is indicated by Sahin et al. (2001).
Maternal antibodies in young chicks have been described to
confer protection against many enteric agents (Clark and
Bueschkens 1988; Pearson et al. 1993; Jacobs-Reitsma et
al. 1995). Anti-C. jejuni antibodies react with multiple
outer membrane components (such as flagellin) of C.
jejuni and kill the organism. This phenomenon is strain
specific and so requires the presence of specific target
antigens on the surface of the organism. Therefore, the
flagellum is required for in vivo colonization. A flagellinbased recom- binant vaccine could be protective against C.
jejuni (Sahin et al. 2001).
The connection between bovine strains of C. jejuni and
campylobacteriosis in humans has been demonstrated by
molecular typing. This causes considerable concern due to
the large numbers of Campylobacter spp. in cattle feces.
The numbers of Campylobacter cells in feces are better
detected (less than 10 CFU/g) by using real-time quantitative polymerase chain reaction (RTQ-PCR) than by using
conventional microbiological methods. Adult humans do
not usually shed C. jejuni for long periods of time (Inglis et
al. 2004).
Inglis et al. (2004) reported the chronic shedding of
Campylobacter spp. in cattle. A high percentage (83%) of
cattle is also contaminated with large quantities of
Campylo- bacter spp. The most prevalent taxa detected
were Cam- pylobacter lanienae (49%) and C. jejuni
(38%). Whether Campylobacter species associated with
cattle are pathogenic to cattle is not well understood.
Strategies for rapid and accurate detection of animals
contaminated with high numbers of Campylobacter cells
are necessary, and removal of those animals may prevent
contamination of equipment and carcasses within the
abattoir. Campylobacter lanienae may be an enteric
pathogen to cattle, and that novel species of Campylobacter
may be chronically shed in large numbers in feces. The fact
that C. lanienae is not typically detected in diagnostic
facilities along with its prevalence in cattle feces raises
questions regarding its potential impact on human health
(Inglis et al. 2004).
Although swine is commonly carrier of Campylobacter
spp., the contamination of carcasses diminishes considerably during the post-slaughter operations, and positive
percentages of 1.3 across all types of retail pork products
have been described. The reduction of Campylobacter spp.
contamination in pork carcasses, occurring sometime
during the chilling process, is attributed to the drying of
the skin (Snijders and Collins 2004).
Marked acquired and cross-resistances of Campylobacter spp. to fluoroquinolones are disquieting: nearly 40% of
human Campylobacter spp. has been found to be resistant

to ciprofloxacin (Olah et al. 2006). Poultry isolates can also

be resistant to tetracyclines and, to a lesser extent,
ciprofloxacin. The resistance of Campylobacter spp. in
poultry meat is therefore of special importance (Ursinitsch
et al. 2004). The rapid emergence of resistances is
attributed to the use of drugs in poultry and other foodproducing animals, and indicates the adaptability of
Campylobacter spp. to adverse conditions (Mead 2004;
Yan et al. 2005). The mechanism of such antimicrobial
resistances could be associated with a system of multi-drug
efflux pumps, which extrudes the antimicrobial agents out
of the bacterial cells (Olah et al. 2006).

Salmonella spp.
Salmonella spp. is an enteric pathogen associated with
animal and slaughter hygiene. In the EU, eggs and egg
products are the most frequently implicated sources of
human salmonellosis. Meat is also an important source,
with poultry and pork implicated more often than beef and
lamb (EFSA 2008). The two most common Salmonella
serotypes are Typhimurium and Enteritidis. In human
salmonellosis, S. Typhimurium is the most frequent
serotype. Salmonella Enteritidis is associated primarily
with poultry and eggs. It has been observed that Salmonella
spp. usually persist during chilling. Human salmonellosis
infections can lead to uncomplicated enterocolitis and
enteric (typhoid) fever, the latter being a serious disease
that may involve diarrhea, fever, abdominal pain, and
headache. Salmonella spp. can also cause systemic infections, resulting in chronic reactive arthritis (Meng and
Doyle 1998; Echeita et al. 1999; DAoust and Maurer
2007).
From 1984 to 2005, there were 17 major outbreaks
of human salmonellosis (S. Typhimurium and S. Enteritidis being involved in, at least, seven of those outbreaks)
from meat, poultry, and derived products, mostly in North
America and Europe. The sources were raw and minced
pork; cooked chicken and turkey; raw, ground, and roast
beef; liver pt, deli meats, kebab, and so on. Six
outbreaks had ca. 100 to 400 confirmed cases, four
outbreaks with ca. 600 to 850 cases, and one outbreak
with >2,100 cases in Spain in 2005 (DAoust and Maurer
2007).
The considerable increase in human foodborne salmonellosis in the 1980s was caused predominantly by S.
Enteritidis PT4 in Europe and PT8 and PT13 in the USA
and Canada. Recently, infections by atypical Salmonella
spp. have been described, e.g., several outbreaks of S.
Enteritidis anaerogenic PT14b (an uncommon phage type)
associated with consumption of contaminated chicken
(Guerin et al. 2006).

Salmonella serotypes have been found to be multidrug resistant, with the spectrum of antibiotic resistance
still increasing; and this high level of resistance can
explain its spread among poultry. However, strains from
swine are often considerably more resistant to antibiotics than strains from other sources. This can be due
to a more intensive use of antibiotics in swine than in
any other animal species. With the sampling protocol
and the diagnostic methods currently used by national
surveillance programs, some infected herds probably
remain undetected, depending on the intensity of the
combined serological and bacteriological testing (Usera
et al. 2002; Rugbjerg et al. 2004). As in Campylobacter
spp., Salmonella acquired and cross-resistances to fluoroquinolones are of great concern because ciprofloxacin is
the treatment of choice for a variety of common foodborne
illnesses (DAoust and Maurer 2007). Salmonella Enteritidis is one of the serotypes most susceptible to displaying
such resistances. There is a connection between the ability
to resist numerous antibiotics and the ability to cause
disease atypical for Salmonella or even more severe
illnesstermed hypervirulence (Carlson 2004).
Unlike S. Enteritidis, DT104 is widely distributed in
the food-producing animal population, especially in cattle.
The pathogen spreads rapidly among animals, of the same
or different species, and to humans. DT104 has been
isolated from a wide range of meat and poultry products:
roast beef, ham, pork sausage, salami, and chicken. An
increase in the prevalence of S. Typhimurium DT104 has
been reported worldwide. Tollefson et al. (1998) stated
that, while less than 1% of all cases of salmonellosis can
be attributed to S. Typhimurium DT104, most multiple
antibiotic-resistant Salmonella isolates are DT104 or a
closely related type; however, the number of cases of
infection with DT104 is continuously growing. The
antibiotic resistance genes of DT104 and related types
are unusually organized as an integron structure, which is
of particular concern because the genes can be retained in
the absence of selective pressure. That structure appears to
have come from a fish pathogen called Pasteurella
piscicida (Carlson 2004). The multi-drug resistance pattern
is to ampicillin, cloramphenicol, streptomycin, sulphonamides, and tetracyclines (ACSSuT pattern) as well as
increasing resistance to trimethoprim and ciprofloxacin
(Meng and Doyle 1998; Acheson 2003). The resistance to
gentamicin, a very active antimicrobial against most
Salmo- nella spp., is also interesting (Echeita et al.
1999). That pattern is present not only in S. Typhimurium
DT104 but also in some other phage types and serotypes,
e.g., DTU302 (Usera et al. 2002). The combination of
multi-resistance towards antibiotics and the ability to
spread rapidly makes DT104 an important public health
problem (Rugbjerg et al.
2004).

Salmonella Typhimurium DT104 hypervirulence has

been described. Hyperinvasion (a transient markedly
increased invasion of intestinal epithelial cells) is probably
a component of DT104 hypervirulence. While a normal
invasion involves only a small fraction of the Salmonella
entering the intestinal cells, for DT104, the majority appear
to invade. After surviving adverse environments, DT104 is
more efficient at invading intestinal cells because such
environments overactivate a gene that initiates invasion
processes. Therefore, hyperinvasion is based on both the
environment and genetic elements. The increased invasion
leads to a more rapid onset of disease, which is more
severe. The human cases of DT104 hypervirulence could be
a result of direct transmission from live cattle (Carlson
2004). Treatments effective against S. Typhimurium appear
to be effective against S. Typhimurium DT104 (Cutter and
Rivera-Betancourt 2000).

Enterohemorrhagic Escherichia coli

Enterohemorrhagic E. coli (EHEC), i.e., E. coli O157:H7
and other serotypes of Shiga toxin-producing E. coli, are
foodborne pathogens of primary concern. They are etiological agents of hemorrhagic colitis. In some cases, complications may occur, e.g., hemolytic uremic syndrome and
thrombotic thrombocytopenic purpura. EHEC other than E.
coli O157:H7 have been increasingly associated with such
complications. The severity of the illness and the low
infective dose (<100 organisms) make E. coli O157:H7
among the most serious foodborne pathogens (Meng and
Doyle 1998; Acheson 2003; Meng et al. 2007).
Escherichia coli O157:H7 is an enteric organism
associated with animal and slaughter hygiene. It may be
present in the feces and intestines of healthy bovines
(McEvoy et al. 2004). Swine and poultry are also possible
reservoirs of E. coli O157:H7 because the organism can
colonize the ceca. The pathogen has also been isolated from
other domestic and wildlife animalssheep, goats, deer,
dogs, horses, and cats (Meng et al. 2007). Therefore, meat
can be contaminated during slaughter operation and
processing (Juneja and Marmer 1999). Most people
infected with E. coli O157:H7 pick up the organism from
cattle, which are a major reservoir, either through direct
contact with feces or by consuming meat or milk (Anon
2004).
The organism is not a rare contaminant in meats. Many
outbreaks of EHEC have been associated with consumption
of undercooked contaminated ground beef. For example,
from 1982 to 2006, there were ca. 15 representative
outbreaks of EHEC from meat and meat products. Most
of those outbreaks was in the USA (among them, one
multi-state outbreak with >700 cases, four deaths), and one

outbreak was in Australia (>200 cases), one in Japan (>100

cases), and one in the UK (>500 cases, 21 deaths). The
sources were undercooked hamburgers, ground beef patty,
roast beef, venison jerky, luncheon and meatballs, salami,
semidry sausage, and so on. Turkey roll has also been
involved in E. coli O157:H7 diseases (Meng and Doyle
1998; Juneja and Marmer 1999; Meng et al. 2007).
Escherichia coli strains from food sources (e.g., animal
carcasses and derived meat products) can harbor potentially
significant virulence determinants, such as cytotoxic necrotizing factors in uropathogenic strains, and cytolethal
distending toxins in strains which are not certain causes of
human infection (Kadhum et al. 2006).
Escherichia coli O157:H7 does not grow at 44.5 C
and has increased acid tolerance. The minimum pH for E.
coli O157:H7 growth is from 4.0 to 4.5 (Meng et al. 2007).
It survives better than Salmonella spp. and Listeria
monocytogenes in acidic foods (Samelis et al. 2001).
Escherichia coli O157:H7 can survive fermentation,
drying, and chill storage in most fermented sausages.
Acid-tolerant-induced cells also can have increased tolerance to other environmental stresses such as heating and
antimicrobials. Escherichia coli O157:H7 has shown
increasing resistance to antibiotics, especially streptomycin, sulfisoxazole, and tetracyclines (Meng et al. 2007). It
is suggested that the use of certain antimicrobials (e.g.,
trimethoprimsulfamethoxazole) for treating EHEC disease can increase the likelihood that a patient develops
other serious complications caused by the organism
(Acheson 2003).
Escherichia coli O157:H7 resistance to heat is not
unusual. However, heating ground beef sufficiently to kill
Salmonella spp. will also kill E. coli O157:H7. Fat has been
found to protect E. coli O157:H7 against heat inactivation
(Meng et al. 2007). From the results of some studies
comparing several meat species (beef, lamb, pork, chicken,
and turkey), the internal temperature required to reduce a
certain number of E. coli O157:H7 log cycles is higher for
ground beef than for the other species. So, D values of E.
coli O157:H7 have been found to be lower in chicken than
in ground beef. Therefore, if ground beef is used to validate
the safety of a process for E. coli O157:H7, that process
will probably also be safe for chicken, turkey, lamb, and
pork (Juneja and Marmer 1999).
Ovomucinglycopeptide has a protective effect against E.
coli O157:H7 infection because of its ability to bind the
organism and so avoid bacterial adhesion to host tissues.
Furthermore, this would allow the use of ovomucinglycopeptide as a probe for the detection of E. coli O157:H7 in
the food hygiene field. Fucosyloligosaccharides have been
found to block the adhesion of other pathogens such as
enteropathogenic E. coli (EPEC) and C. jejuni (Kobayashi
et al. 2004).

Listeria monocytogenes
Listeria monocytogenes is an environmentally transmitted
pathogen. It is a psychrotroph and ubiquitous, and grows
well in poor substrates, which enables contamination
during any phases
of
food
chain.
Listeria
monocytogenes is able to survive and multiply on plants
and in soil and water. The incidence of listeriosis is
relatively low, but it is of major public health concern
because of the severity and non-enteric nature of the
disease,
which
reveals
as
meningitis
or
meningoencephalitis, septicemia, and abortion, mainly
in populations such as young children, the elderly,
pregnant women, and other immunocompromised persons.
It is also a major public health concern because of the
ability of the pathogen to grow at refrigeration
temperature. Pediatric lymphocytic meningoencephalitis
due to L. monocytogenes is a serious form of brain
infection, even in immunocompe- tent childhood,
especially when an important inflammatory syndrome
appears. Most persons frequently ingest listeriae, but they
are apparently resistant to infection (Meng and Doyle
1998; Flodrops et al. 2005; Swaminathan et al. 2007). The
infective dose depends on the immunological status of the
human host and characteristics of the organism such as its
virulence factors. The dose is usually high, but in some
cases it may be as low as several hundred or even less
organisms (Acheson 2003; Swaminathan et al. 2007).
Cooked, ready-to-eat meat and poultry products have
been the source of sporadic and outbreak-associated cases
of listeriosis in North America and Europe. Contaminated
frankfurters and turkey deli meat caused multi-state outbreaks of listeriosis in the USA in 1998, 2000, and 2002
(Swaminathan et al. 2007).
Thus, ready-to-eat meals, unreheated frankfurters, and
undercooked chicken can be vehicles for the pathogen. It
has been found that 16% of salamis are contaminated
with the pathogen (Hutchins 1996). The organism tends to
concentrate in organs. Therefore, eating undercooked organ
meat may be more hazardous than eating undercooked
muscle tissue (Meng and Doyle 1998; Swaminathan et al.
2007).
Listeria monocytogenes is not significantly affected by
vacuum packaging and certain modified atmospheres
because it is a facultative anaerobe. There is very little or
no L. monocytogenes multiplication at ca. pH 5.0 (Glass
and Doyle 1989). The organism grows well in some
refrigerated ready-to-eat foods if stored for a long period,
and thus consumer practices may determine the level of L.
monocytogenes. Ready-to-eat meat and poultry products
that have received heat treatment followed by cooling in
brine before packaging may provide a particularly
favorable environment for L. monocytogenes because of the
reduction of competitive microbiota and the high salt
tolerance of the organism. Therefore, ready-to-eat foods
are of great risk

and it is not practical to expect them to be L. monocytogenes free (Swaminathan et al. 2007).
If industries do not report positive findings, the
incidence of the pathogen is underestimated, and therefore
the Administration keeps the zero-tolerance policy, which
has been questioned by industries of many countries as
unattainable. Food regulatory agencies in many countries
have accepted the argument that it is impossible to produce
L. monocytogenes-free foods and have given tolerance
levels for the pathogen. For this reason, levels of risk for
different meat and poultry products have been established.

Other Emerging Pathogenic Bacteria

Arcobacter butzleri formerly belonged to the genus Campylobacter. It is a potential foodborne pathogen, being
involved in enteric diseases and also extraintestinal
invasive diseases such as septicemia and bacteremia. It can
be present in surface and ground waters and sewage. In
fact, water is supposed to play an important role in the
transmission of the organism, with drinking water being a
major risk factor in acquiring diarrheal illness by Arcobacter spp. Raw poultry, pork, beef, and meat products are
also sources of A. butzleri infection. Arcobacter spp., like
Campylobacter spp., have been reported more frequently
from poultry than from red meats. Carcass contamination
has several sources, other than slaughter equipment. The
pathogen has been found to be cytotoxic, but its role in
causing illness is not fully understood yet. Arcobacter spp.
differ from Campylobacter spp. in their ability to grow
aerobically at 15 C. Arcobacter butzleri can grow between
pH 5.0 and 8.5, but not at temperatures above 40 C. Its
viability decreases gradually under refrigeration (Wesley
1997; Meng and Doyle 1998; Hilton et al. 2001; VillarruelLpez et al. 2003; Moreno et al. 2004; Rivas et al. 2004;
Lehner et al. 2005).
Mycobacterium avium subsp. paratuberculosis (M. paratuberculosis) can be transmitted by ingestion of raw and
processed meats. Because of the similarities with paratuberculosis, a mycobacterial origin of Crohns disease, a
chronic intestinal enteritis, is suggested, although the role
of M. paratuberculosis in the disease is controversial yet.
It is known that the organism may contribute to Crohns
disease, but the etiology is still to be confirmed in some
cases of the disease (Hermon-Taylor 2001; Naser et al.
2004).
Aeromonas hydrophila infection has water as the
primary source. However, large populations of aeromonads
have been found in products such as minced beef, pork, and
chicken, smoked sausage, liver pt, and cooked ham.
Aeromanas spp. are the etiological agents in a variety of
extraintestinal diseases (e.g., peritonitis, endocarditis, pneumonia, conjunctivitis, and urinary tract infections) involv-

ing immunocompetents as well as immunocompromised

individuals. Some strains are enteropathogenic (Galindo
and Chopra 2007).
Enterobacter sakazakii is mainly transmitted through
consumption of rehydrated contaminated milk powder
infant formulae, and is involved in serious diseases such as
neonatal meningitis, bacteremia, necrotizing enterocolitis,
appendicitis, and conjunctivitis. The pathogen is not a
usual pathogen associated with meat and poultry, although
it has been isolated from minced beef, cured meats, and
sausage meat (Iversen and Forsythe 2003; Gurtler et al.
2005).
Helicobacter pylori is quite fragile and does not develop
well outside of its host. The organism has been found in
water but not in foods. It is difficult to detect by
conventional techniques, so molecular methods have been
used. The organism is associated with gastric ulcers and
cancer. It is suggested that there is the possibility of
transmission of Helicobacter pullorum from poultry (with
the organism being in the intestinal tract and liver) to
humans, in which the pathogen causes gastroenteritis and
liver disease. As the organism is microscopically similar to
Campylobacter coli, it could be overlooked as a cause of
enteritis. Some human H. pullorum isolates produce the
cytolethal distending toxin (Wesley 1997; Meng and Doyle
1998; Ceelen et al. 2006).

Conclusions
Careful food production, handling of raw products, and
preparation of finished foods are the bases for prevention
from and control of emerging pathogens. In particular, for
meat and poultry production, it is essential that hygiene be
maintained during slaughter operations according to
HACCP principles and codes of good manufacturing
practices to reduce the risk of carcass contamination.
Effective epidemiological surveillance and control programs by public health authorities are required to reduce
the prevalence of emerging pathogens in the food chain.
Education of food handlers and consumers in food safety
principles is also essential.
Prudent use of antimicrobials may prolong their effectiveness by preventing a serious public health problem such
as antibiotic acquired and cross-resistances in some
pathogenic bacterial strains.

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